The Jugular Foramen: Imaging Strategy and ORIGINAL RESEARCH Detailed Anatomy at 3T

Published October 2, 2008 as 10.3174/ajnr.A1281 The Jugular Foramen: Imaging Strategy and ORIGINAL RESEARCH Detailed Anatomy at 3T

J. Linn BACKGROUND AND PURPOSE: The purpose of this study was to assess how well the anatomy of the F. Peters jugular foramen (JF) could be displayed by 3T MR imaging by using a 3D contrast-enhanced fast imaging employing steady-state acquisition sequence (CE-FIESTA) and a 3D contrast-enhanced MR B. Moriggl angiographic sequence (CE-MRA). T.P. Naidich H. Bru¨ ckmann MATERIALS AND METHODS: Twenty-five patients free of skull base lesions were imaged on a 3T MR imaging scanner using CE-FIESTA and CE-MRA. Two readers analyzed the images in collaboration, I. Yousry with the following objectives: 1) to score the success with which these sequences depicted the glossopharyngeal (CNIX) and vagus (CNX) nerves, their ganglia, and the spinal root of the accessory nerve (spCNXI) within the JF, and 2) to determine the value of anatomic landmarks for the in vivo identification of these structures.

RESULTS: CE-FIESTA and CE-MRA displayed CNIX in 90% and 100% of cases, respectively, CNX in 94% and 100%, and spCNXI in 51% and 0% of cases. The superior ganglion of CNIX was discernible in 89.8% and 87.8%; the inferior ganglion of CNIX, in 73% and 100%; and the superior ganglion of CNX, in 98% and 100% of cases. Landmarks useful for identifying these structures were the inferior petrosal sinus and the external opening of the cochlear aqueduct.

CONCLUSIONS: This study protocol is excellent for displaying the complex anatomy of the JF and related structures. It is expected to aid in detecting small pathologies affecting the JF and in planning the best surgical approach to lesions affecting the JF.

he jugular foramen (JF) is a bony channel that transmits dural sheath as CNX, but remains separate from it.4 Just infe- Tvessels and cranial nerves IX, X, and XI (CNIX, CNX, and rior to its dural meatus, CNIX turns forward and then sharply CNXI) through the skull base into the carotid space.1 It can be downward forming the so-called “genu” of CNIX.1 divided into 3 compartments1: 1) a neural compartment, con- Despite extensive cadaveric dissection studies, which have NECK & HEAD taining the CNIX to CNXI; 2) a larger venous compartment addressed the anatomy of the JF, many details on the in vivo (sigmoid part), containing the sigmoid sinus; and 3) a smaller anatomy of the JF remain unclear.1-7 Due to its complexity, to venous compartment (petrosal part), containing the inferior our knowledge, the JF anatomy has not yet been systematically petrosal sinus. The sigmoid and the petrosal parts are sepa- evaluated in imaging studies, though this knowledge would be rated by bony processes: the intrajugular processes, which highly important for presurgical planning. originate from the opposing surfaces of the temporal and oc- To date, high-resolution MR imaging provides a noninva- RESEARCH ORIGINAL cipital bones, as well as by a dural septum, which connects sive tool, which should enable us to depict the exact location of these 2 bony structures.1 the intraforaminal structures in vivo. Recent studies showed The lower cranial nerves enter the JF via 2 dural meatuses: that contrast-enhanced steady-state and MR angiography the glossopharyngeal meatus for the glossopharyngeal nerve (MRA) sequences are suitable techniques to image the intrafo- (CNIX) and the vagal meatus for both the vagus nerve (CNX) 7,8 and the accessory nerve (CNXI). CNIX and CNX each possess raminal segments of other cranial nerves, but not yet CNIX– both a superior (supCNIX and supCNX) and an inferior CNXI. Therefore, we hypothesized that a contrast-enhanced ganglion (infCNIX and infCNX). While the supCNIX, the 3D fast imaging employing steady-state acquisition sequence infCNIX, and the supCNX lie within the JF, the infCNIX is (CE-FIESTA) and a high-resolution contrast-enhanced gradi- located more caudally.2,3 The cranial nerve roots of CNXI ent-echo MRA (CE-MRA) technique, performed on a 3T MR (crCNXI) intermingle with the roots of CNX within the JF, so imaging scanner, should be valuable for the identification of their fibers are classified together as the CNX/XI complex.1 the JF and its contents. The spinal root of CNXI (spCNXI) traverses the JF in the same Thus, we aimed to determine the potential of these sequences in providing detailed information on the MR imaging Received June 10, 2008; accepted July 12. anatomy of the JF. From the Department of Neuroradiology (J.L., F.P., H.B., I.Y.), University Hospital Munich, Munich, Germany; Institute of Anatomy, Histology, and Embryology (B.M.), Medical Uni- versity Innsbruck, Austria; and Department of Radiology, Section of Neuroradiology (T.P.N.), Materials and Methods Mount Sinai Medical Center, New York, NY. Patients Paper previously presented in part at: European Congress of Radiology, March 8, 2008; Vienna, Austria; Deutschen Ro¨ntgenkongress, October 17–19, 2008; Berlin, Germany; and The study group comprised 25 patients (16 women; mean age, 50 Ϯ Jahrestagung der Deutschen Gesellschaft fu¨r Neurochirurgie, September 20, 2008; Wu¨rz- 17 years) in whom contrast-enhanced MR imaging was performed for burg, Germany. unrelated reasons and who agreed to undergo additional CE-FIESTA Please address correspondence to Jennifer Linn, MD, Department of Neuroradiology, and CE-MRA sequences. None of these patients had known clinical University Hospital Munich, Marchioninistr 15, D-81377 Munich, Germany; e-mail: [email protected] abnormalities affecting the skull base or the infratentorial region. Fur- DOI 10.3174/ajnr.A1281 thermore, we present 1 illustrative case of a patient with a meningi-

AJNR Am J Neuroradiol ●:● ͉ ● 2009 ͉ www.ajnr.org 1 Copyright 2008 by American Society of Neuroradiology. Table 1: Sequence parameters CE-FIESTA CE-MRA TR (s) 4.5 6.6 TE (s) 1.8 2.3 FOV (mm) 160 180 Flip angle (°) 50 20 Matrix (mm) 256 ϫ 256 450 ϫ 450 Section thickness (mm) 0.6 0.8 NEX 2 1.15 Resolution (mm) 0.6 ϫ 0.6 ϫ 0.6 0.4 ϫ 0.4 ϫ 0.8 Duration (min:s) 7:45 7:15 Note:—CE-FIESTA indicates contrast-enhanced fast imaging employing steady-state acquisition; CE-MRA, contrast-enhanced MR angiography. oma affecting the lower cranial nerves and the JF to illustrate the clinical relevance of these MR images. The study was approved by the review board of our department and conformed to the Helsinki declaration. All patients gave in- formed consent to participate before beginning the study. Fig 1. Petrosal and sigmoid parts of the JF. Axial CE-MRA image demonstrates the petrosal and sigmoid parts of the JF as well as the cranial nerves within the intrajugular MR Imaging compartment. The thick white arrow marks the right interjugular process of the occipital Imaging was performed on a 3T MR imaging scanner by using an bone; the black arrow depicts the dural septum between the petrosal and sigmoid part of the JF. Asterisks mark the drainage of the inferior petrosal sinus into the jugular bulb 8-channel high-definition head coil (GE Healthcare, Milwaukee, between CNIX anterolaterally (dotted arrows) and the CNX/XI complex at the level of the Wis). The imaging protocol consisted of a CE-MRA and a CE-FIESTA supCNX posteromedially (thin white arrow). 1 indicates the ICA; 2, the inferior petrosal sequence. The CE-MRA was performed first and started 30 seconds sinus; 3, the sigmoid sinus. after the administration of 0.1-mmol/kg gadobenate dimeglumine (sequence parameters are given in Table 1). The infCNIX was identified by its anatomic location approximately 3 mm inferior to the supCNIX.3 The supCNX was identified Image Analysis by its position immediately caudal and dorsal to the supCNIX.2,3 The The 3D datasets from both sequences were analyzed collaboratively infCNX was not assessed in this study because it lies further caudally by 2 experienced neuroradiologists on a standard workstation by us- along the course of CNX and not within the JF.1,3 ing the multiplanar reconstruction function. Ratings were reached by Cochlear Aqueduct. The maximal width of the external opening consensus. The left and right sides of each patient were assessed of the cochlear aqueduct was measured on an oblique plane that was separately. reconstructed parallel to the course of the aqueduct. The length of the The certainty of identifying each anatomic structure was scored cochlear aqueduct was measured from the external opening of the on both MR images separately and recorded on an arbitrary scale of aqueduct as far proximal as the aqueduct could be traced toward the 0–2 (identified with certainty, 2; most probably identified, 1; and not cochlea (length of the aqueduct). identified, 09). Adjacent Cranial Nerves: CNVII and CNXII. The certainty of Intraforaminal Compartments. To assess the value of the 2 se- identifying the facial nerve (CNVII) in its course through the tempo- quences in depicting the different intraforaminal compartments, we ral bone to the parotid gland and of the canalicular segment of the identified the intrajugular processes of the temporal and occipital hypoglossal nerve (CNXII) was assessed. Furthermore, we evaluated bones and the dural septum between them. The maximum antero- whether a single or a duplicated hypoglossal canal was present. posterior and transverse dimensions of the sigmoid compartment and the maximum diameter of the inferior petrosal sinus proximal to Statistical Analysis its drainage into the petrosal portion of the JF were measured on To compare the value of the 2 sequences for the identification of each transverse reconstructed planes of the CE-MRA. anatomic structure, we performed the Fisher exact probability test. P CNIX, CNX/XI, and spCNXI within the JF. The exact position of values Ͻ .05 were judged to be significant. the nerves within the neural compartment, their spatial relationships to each other, and the visualization of a “genu” of CNIX were also Results assessed. Forty-nine of 50 sides were suitable for analysis. In 1 patient, Ganglia of CNIX and supCNX. The success of identifying the CE-FIESTA revealed an asymptomatic small arachnoid cyst in cranial nerve ganglia was scored as follows: A score of 2 was assigned the perimedullary cistern on the right side, which distorted the if the ganglion was discernible as a circumscribed thickening of the cisternal segments of the lower cranial nerves. This single side appropriate cranial nerve. A score of 1 was assigned if no thickening of was excluded from further analysis. the nerve was depicted but the nerve itself could be identified with certainty at the anatomic site of its ganglion. A score of 0 was assigned Intraforaminal Compartments if neither the ganglion nor the nerve could be identified at the appro- On both sequences, the 3 intraforaminal compartments could priate site. be identified by reliably depicting the temporal and occipital For the identification of the supCNIX, we used 2 landmarks: 1) the intrajugular processes as well as the dural septum separating external opening of the cochlear aqueduct1,10 and 2) the “genu” of the petrosal from the sigmoid portion. CE-MRA was superior CNIX.1 to CE-FIESTA for identifying the dural septum (89.9% versus

2 Linn ͉ AJNR ● ͉ ● 2009 ͉ www.ajnr.org Table 2: Identification of anatomic structures within and adjacent to the jugular foramen*

Anatomic Structure CE-FIESTA CE-MRA (49 sides) 2 1 0 Total† 2 1 0 Total† Dural septum 0 (0) 21 (43) 28 (0) 21 (43) 29 (59.1) 15 (30.6) 5 (10.2) 44 (89.9) Cranial nerves CNIX 36 (73.5) 8 (16.3) 5 (10.2) 44 (90) 49 (100) 0 (0) 0 (0) 49 (100) CNX/XI complex‡ 39 (79.6) 7 (14.3) 3 (6.1) 46 (94) 49 (100) 0 (0) 0 (0) 49 (100) spCNXI 10 (40) 6 (24) 9 (36) 25 (51) 0 (0) 0 (0) 49 (100) 0 (0) Cochlear aqueduct 49 (100) 0 (0) 0 (0) 49 (100) 33 (67) 16 (33) 0 (0) 49 (100) Ganglia supCNIX 12 (24.5) 32 (65.3) 5 (10.2) 44 (89.9) 13 (26.6) 30 (61.2) 6 (12.2) 43 (87.8) infCNIX 0 (0) 36 (73) 13 (26.5) 36 (73) 24 (0) 25 (100) 0 (0) 49 (100) supCNX 0 (0) 48 (98) 2 (4) 48 (98) 0 (0) 49 (100) 0 (0) 49 (100) Adjacent cranial nerve CNVII 33 (67.3) 10 (20.4) 6 (12.2) 43 (87.6) 20 (40.8) 8 (16.3) 21 (42.9) 28 (57.1) Hypoglossal canal 49 (100) 0 (0) 0 (0) 49 (100) 49 (100) 0 (0) 0 (0) 49 (100) CNXII within canal 46 (93.9) 3 (6.1) 0 (0) 49 (100) 49 (100) 0 (0) 0 (0) 49 (100) Note:—sup indicates superior; inf, inferior. * Data are numbers of sides (percentage). † Total number of sides (percentage) on which the respective anatomic structure was identified (score of 1 or 2). ‡ The cranial nerve rootlets of CNXI intermingle with CNX inside the JF, and thus these nerves are referred to as the CNX/XI complex.

Fig 2. The cranial nerves and their ganglia within the JF. Consecutive axial CE-MRA images from the cranial-to-caudal direction depict the CNIX and the CNX/XI complex within the JF. A, The most cranial section is located on the level of the right supCNIX and the left infCNIX (crossed arrow). Note that in this case, no circumscript thickening of the nerve is identifiable. Thin white arrows indicate the inferior petrosal sinus; 1, the ICA; 2, the sigmoid sinus. B, Section at the level of the supCNIX (thick arrows). Crossed arrows indicate CNIX within the JF; thin white arrows, the inferior petrosal sinus; 1, the ICA; 2, the sigmoid sinus. Note that the right sigmoid part (2Ј) is significantly larger than the left one (2) in this case.

Table 3: Diameters of the inferior petrosal sinus and sigmoid jugular fossa in 51% of sides (Fig 3 and Table 2). On CE-MRA portion* sequences, the spCNXI could not be identified in its cisternal Structure Right Side (mm) Left Side (mm) course, so it could not be traced distally. Of the 3 cranial nerves, CNIX was located most anterorolaterally. CNX/XI adjoined it Inferior petrosal sinus† 3.5 (2.3–5.5) 3.6 (2–5.7) Sigmoid part† posteromedially. Where identified, the spCNXI lay further pos- Anteroposterior 8.7 (8–9.4) 7.7 (6.9–8.5) teromedially. The CNX/XI complex typically had a triangular Left-right direction 10 (9.3–10.7) 8.8 (8–9.6) shape on transverse sections (Figs 1 and 2). * Data are mean (range). † Measured on CE-MRA. Nerve Ganglia 43%; Fig 1 and Table 2). The sigmoid portion was significantly The nerve ganglia could be reliably identified in high percentages larger on the right than on the left side in 60% of patients, on both the CE-FIESTA and CE-MRA sequences: supCNIX, whereas there was no significant difference between the mean 89.9% and 87.8%; infCNIX, 73% and 100%; supCNX, 98% and width of the inferior petrosal sinus on either side (Fig 2 and 100%, respectively (Figs 1, 2, 4, and 5). CE-MRA was superior to Ͻ Table 3). the CE-FIESTA for identifying the infCNIX (P .05). There was no significant difference between the sequences with respect to Cranial Nerves within the Neural Compartment displaying supCNXI and supCNX (Table 2). Both pulse sequences enabled us to identify and differentiate CNIX from CNX/XI within the neural compartment of the Cochlear Aqueduct jugular fossa (FIESTA, 90% and 94%; CE-MRA, 100% and Both sequences depicted the cochlear aqueduct and its exter- 100%, respectively). However, the CE-MRA sequence proved nal opening on both sides (Table 2). For the dimensions of the to be significantly superior to the CE-FIESTA (P Ͻ .01; Fig 2 cochlear aqueduct, see Table 4. and Table 2). In all cases in which CNIX was discernible within the JF, its genu could also be identified on both sequences. Cranial Nerves Adjacent to the JF: CNXII and CNVII CE-FIESTA images provided better depiction of the spCNXI The canalicular segments of CNXII could be reliably identified than did CE-MRA. On CE-FIESTA images, the spCNXI could be in both sequences (Fig 5 and Table 2). In 5 sides (10.2%), the followed from the brain stem through the vagal meatus into the hypoglossal canal was duplicated (Fig 6); in the remaining

AJNR Am J Neuroradiol ●:● ͉ ● 2009 ͉ www.ajnr.org 3 Fig 3. A and B, Depiction of the spCNXI on FIESTA MR imaging. The spCNXI (thin white arrows) is visualized on axial (A) and oblique coronal (B) FIESTA MR images in its cisternal course (thin arrows) and after its entrance into the JF (crossed arrow). The dotted arrow indicates the CNX/XI complex.

Fig 4. Visualization of the supCNIX. Axial (A) and oblique sagittal (B) 3D-FIESTA MR images. B, The oblique sagittal image is reconstructed parallel to the cisternal course of the lower CNIXs. Nerve root bundles of CNIX (thin white arrows), CNX (crossed white arrows), crCNXI (black arrow), and CNXII (black arrowhead) and the glossopharyngeal meatus (white arrowhead), vagal meatus (thick white arrow), and the supCNXI (dotted white arrows) are depicted.

Fig 5. A and B, CNXII within the hypoglossal canal. Axial FIESTA MR image (A) and CE-MRA image (B) clearly demonstrate the canalicular segment of CNXII. Dotted arrows indicate borders of the hypoglossal canal; crossed arrows, the canalicular segment of CNXII; thin white arrows, the CNX/XI complex within the JF; 1, the ICA; 2, the jugular bulb.

Table 4: Dimensions of the cochlear aqueduct* Discussion This is the first 3T MR imaging study to provide detailed in- Right Side (mm) Left Side (mm) formation on the anatomy of the JF and its contents. Our Length 6.3 (3.6–9.5) 6.4 (3.8–8.7) Width of external opening 2.9 (1.2–5.2) 2.8 (2–5.1) results show that combined use of CE-FIESTA and CE-MRA successfully depicts the complex anatomy of the JF, its con- * Data are mean (range) measured on CE-FIESTA. tents, and adjacent structures. Although CE-MRA proved to be significantly superior to sides, a single canal was present. CNVII was depicted in its CE-FIESTA for identifying and differentiating the intrafo- course through the temporal bone to the parotid gland, with raminal portions of CNIX and CNX/XI, only the CE-FIESTA the CE-FIESTA being superior to the CE-MRA (P Ͻ .01, 88% sequence differentiated the spCNXI from CNX/XI. Our pro- versus 57%; Fig 7 and Table 2). tocol enabled us to visualize the ganglia of CNIX and CNX within the JF for the first time. Both contrast-enhanced pulse Illustrative Case sequences reliably depicted the glossopharyngeal and vagal We present a 52-year-old male patient with a left-sided me- ganglia, but the CE-MRA was superior to the CE-FIESTA for ningioma of the petrosellar ligament, which extends through- displaying the infCNIX. out the lateral cerebellomedullary cistern as far caudal as the The JF is one of the most complicated anatomic structures level of the hypoglossal canal. CE-MRA and FIESTA images of the skull base. Although several anatomic dissection studies depicted the lower cranial nerves and their ganglia with respect have evaluated its anatomy,1-3 few in vivo imaging studies to the tumor extension in detail (Fig 8). have been reported in the literature.9-14 These imaging studies

4 Linn ͉ AJNR ● ͉ ● 2009 ͉ www.ajnr.org Fig 6. Demonstration of a bilaterally duplicated hypoglossal canal. Oblique reconstructed FIESTA images of a patient with a duplicated hypoglossal canal on both sides. Thumbnails indicate the reconstruction planes. Open thick arrows indicate borders of the caudal part of the duplicated canal; crossed arrows, the canalicular segments of the hypoglossal nerves. Note that 2 distinct canalicular nerve root bundles can be identified, both of which are demonstrated simultaneously in the images (crossed arrows). B, Dotted arrow indicates the bony septum between both the cranial and the caudal parts of the duplicated hypoglossal canal.

Fig 7. Depiction of CNVII. Axial FIESTA (upper row) and CE-MRA images demonstrate CNVII (thin white arrows indicate the right CNVII; crossed arrows, the left CNVII) within the stylomastoid foramen (A) and in its extracranial course after leaving the temporal bone via the stylomastoid foramen (B and C). 1 indicates the styloid process of the temporal bone; 2, the sigmoid sinus (A) and jugular vein (B and C), respectively; 3, the ICA. did not analyze the complex intraforaminal anatomy in detail. These sequences have usually been used to image the cisternal Therefore, the diagnosis of intraforaminal pathologic pro- segments of the cranial nerves.18-20 When used after intrave- cesses remains a challenge. The aim of the present study was to nous contrast enhancement, however, they also provide suffi- address this problem. cient contrast to enhance the venous plexus surrounding the intraforaminal portions of the nerves.8,15 As a result, the Sequences nerves appear as nonenhancing linear structures within the Recent studies showed that contrast-enhanced steady-state se- enhancing plexus. By use of these sequences, both the cisternal quences such as 3D constructive interference in steady-state and the intraforaminal portions of the nerves can be imaged in and 3D FIESTA can be used successfully to image the intrafo- 1 session. raminal and cavernous segments of the cranial nerves.8,15-17 The image contrast provided by the steady-state sequences

AJNR Am J Neuroradiol ●:● ͉ ● 2009 ͉ www.ajnr.org 5 Fig 8. Illustrative clinical case. A 52-year-old male patient with a left-sided meningioma of the petrosellar ligament (marked as 1). A and B, The meningioma extends throughout the lateral cerebellomedullary cistern as far caudal as the level of the hypoglossal canal. CE-MRA (A) and FIESTA (B) images allow the detailed depiction of the lower cranial nerves and their ganglia with respect to the tumor extension. A, Axial CE-MRA image shows the meningioma (1) which spreads around the spCNXI (thin white arrow). Black arrows indicate the hypoglossal nerve within the hypoglossal canal; open thick white arrow, supCNX; dotted white arrow, the dural septum between the petrosal and jugular part of the JF; 2, vertebral arteries. Note that a brain stem arteriovenous malformation is also present as an incidental finding in this patient (marked as 3). B, FIESTA images reconstructed in a considerably oblique plane aligned precisely along the anatomic course of the cisternal segment of the glossopharyngeal nerve root bundle (dotted white arrows) and the vagal nerve root bundle (thin white arrows). The crossed arrows mark supCNIX, whereas the thick open arrows delineate the supCNX. 1 indicates a meningeoma; 2, the vertebral artery. appears to be weaker than the contrast provided by contrast- entiation of spCNXI from the CNX/XI complex, which was enhanced T1-weighted sequences such as 3D magnetization- not possible with the use of CE-MRA. prepared rapid acquisition of gradient echo and MRA.8,15 For Our results support recent anatomic studies that question example, it has been shown that contrast-enhanced time-of- the presence of an intracisternal or intraforaminal connection flight (TOF) MRA is a useful tool to image the trigeminal between the crCNXI nerve root bundles and spCNXI and ganglion due to its strong venous enhancement.15 Compared demonstrate a tight connection between CNX and crCNXI with TOF-MRA, CE-MRA is less prone to flow-related signal- within the JF.4,24 intensity loss,21 while also providing excellent arterial and venous contrast.22 Here for the first time, we made use of high- Compartments of the JF resolution CE-MRA to image the cranial nerves and to According to Rhoton,1 the JF may be subdivided into 3 com- compare it to CE-FIESTA for the depiction of the JF and its partments: 1 neural or intrajugular compartment (pars ner- content. vosa) and 2 venous compartments, which are partially separated by the intrajugular processes of the temporal and Identification of CNIX, CNX, and CNXI within the JF occipital bones and by dural septa. The venous compartments CNIX enters the JF through a dural channel called the glosso- consist of the larger posterolateral sigmoid compartment, pharyngeal meatus. Soon thereafter, CNIX abruptly turns for- which receives the flow of the sigmoid sinus, and a smaller ward and makes a 90° curve, the so-called genu of CNIX.23 anteromedial petrosal compartment, which receives drainage CNX and CNXI enter the JF together via the vagal meatus. from the inferior petrosal sinus. The pars nervosa, which con- This dural channel lies posterior to the glossopharyngeal me- tains CNIX–CNXI, is situated between the sigmoid and petro- atus. The vagal meatus is located inferior to the glossopharyn- sal compartments.1,2 geal meatus on the medial wall of the JF and is separated from In accordance with these anatomic findings, we could de- the glossopharyngeal meatus by a dural septum.23 At the dural pict the intrajugular processes and the dural septum separat- orifice of the JF, the nerve roots of CNX and crCNXI inter- ing the petrosal from the sigmoid compartments. We found mingle; the 2 roots become indistinguishable and cannot be that the cranial nerves aligned between the venous compart- separated from each other by microdissection.2 Thus, CNX ments along a trajectory from anterolateral (CNIX) to pos- and crCNXI are referred to as the CNX/XI complex. teromedial direction (first, the CNX/XI complex and, second, CE-FIESTA and CE-MRA both provided excellent contrast the spCNXI). and resolution within the JF. Both sequences could be used to identify the nerves as nonenhancing linear structures coursing Cochlear Aqueduct through the surrounding enhancing venous structures. Both The cochlear aqueduct houses the perilymphatic duct and a sequences could be used to differentiate between CNIX and tubular prolongation of the dura mater that is filled with the CNX/XI complex within the foramen. However, CE-MRA CSF. The external opening of the aqueduct is located medial proved to be superior to CE-FIESTA in this respect, due to the to the jugular fossa and above the level of the petrosal fos- stronger and more homogeneous contrast of the surrounding sula. Thus, it lies immediately adjacent to the entrance venous plexus provided by CE-MRA. porus of CNIX and just cranial to the supCNIX.23 The co- On the other hand, the CE-FIESTA provided excellent de- chlear aqueduct is widest where it lies closest to CNIX and piction of the cisternal courses of the cranial nerves. On CE- narrows toward the cochlea.25,26 CE-FIESTA was superior FIESTA sequences, the cranial nerves can be followed from to CE-MRA in depicting the aqueduct, most probably due their exit at the brain stem through the cisterns into their re- to the high signal intensity of CSF on CE-FIESTA. Ana- spective meatuses and through the JF. Therefore, both cister- tomic dissection studies showed that the cochlear aqueduct nal and intraforaminal nerve segments can be imaged by use of is not patent in most cases (60%–67%25). Not surprisingly, a single sequence. Thus, the CE-FIESTA facilitated the differ- therefore, CE-FIESTA studies, in vivo, showed the full

6 Linn ͉ AJNR ● ͉ ● 2009 ͉ www.ajnr.org length of the aqueduct in only 27%. This difference most alize the variations of this drainage into the jugular bulb. The likely is the result of the difficulty of MR imaging in dis- mean width of the distal inferior petrosal sinus was deter- playing the very narrow (0.1-mm-diameter) portion of the mined to be 3.5 mm in our study, which is in accord with aqueduct near the cochlea.26 anatomic dissection studies (2–4 mm29).

Ganglia Relationship to Adjacent Cranial Nerves To the best of our knowledge, this is the first in vivo imaging Several important anatomic structures traverse the skull base study that assesses the visualization of the ganglia of CNX and in close vicinity to the JF. These are namely the internal carotid CNX in detail. artery (ICA) anteriomedially, the CNVII laterally, and the The supCNIX is located within a small dural pocket just at CNXII inferolaterally. Detailed knowledge of these spatial re- the point where CNIX pierces the dura of the glossopharyn- lationships is essential in neurosurgical approaches to the JF.1 geal meatus. It has a mean diameter of 1.5 mm and is macro- CNXII joins CNIX-XI when exiting the JF and courses ad- scopically visible as a circumscribed thickening of the nerve in jacent to the vagus nerve. The extracranial opening of the hy- only one third of cases.1 Using the external opening of the poglossal canal is typically located medial to the pars nervosa cochlear aqueduct and the genu of CNIX as landmarks,1,23 we of the JF,1 which could always be detected with both sequences identified the supCNIX on CE-FIESTA and CE-MRA in 90% and 88% of sides, respectively. equally well. CE-FIESTA and CE-MRA allowed detailed eval- The infCNIX can be detected approximately 3 mm inferior uation of the relationship between the CNXII and the nerves 30 to the supCNIX3 and is the origin of the tympanic nerve (Ja- of the JF. In accordance with anatomic dissection studies, we cobson nerve). CE-MRA was superior to the CE-FIESTA in observed a duplicated canal in 10% of sides, a finding that has visualizing the infCNIX (100% versus 73%). This is explained not yet been described in MR imaging studies. by the more homogeneous venous contrast in CE-MRA. CNVII crosses the lateral surface of the styloid process ad- The supCNX is seen as an expansion of CNX just distal to jacent to the JF. The close spatial relationship between CNVII where its rootlets gather at the intracranial side of the foramen. and the JF is of particular importance in the postauricular It is about 2.5 mm in length and ends at the extracranial side of transtemporal approach, the most commonly used surgical the foramen.1,2 We could always identify the CNX/XI complex route for lesions extending through the JF.1 CE-MRA and par- at the anatomic site of this ganglion (score of 1), whereas we ticularly the CE-FIESTA sequence enabled us to visualize the never observed a clearly defined thickening of the nerve. This CNVII in its complete course through the temporal bone to is in accordance with the fact that the supCNX is macroscop- the parotid gland and thus might facilitate presurgical plan- ically visible as a circumscribed thickening of the nerve in only ning of lateral approaches.1,2 one sixth of cases.1 Both CE-MR imaging sequences depicted the supCNX well. Limitations of the Protocol The auricular branch of CNX (Arnold nerve) arises from One limitation of our protocol might be the duration of ap- CNX at the level of the supCNX. Although Jacobson and Ar- proximately 15 minutes if both sequences are performed. In nold nerves were not directly assessed in this study, the infCNIX and the supCNX provide landmarks for localizing patients with reduced compliance, this will probably result in a the site of their origin. Because Arnold and Jacobson nerves reduced imaging quality. In such cases, we recommend choos- may be related to glomus tumors, depiction of the sites of ing one of the sequences, depending on the pathologic condi- origin of these nerves could have clinical significance.1,27 The tion that is suggested. If the JF itself is affected, CE-MRA inferior ganglion of CNX was not analyzed in this study be- should be performed as the first line; if the pathology predom- cause it is not located within the JF, but more caudally along inately affects the cisternal part of the lower cranial nerves, the the course of CNX. FIESTA sequence should be chosen.

Jugular Bulb and Inferior Petrosal Sinus Implications for Patient Care The jugular bulb and the JF are usually larger on the right side, A wide variety of pathologic processes affect the JF (eg, glomus reflecting the larger diameter of the sigmoid sinus on the jugulare tumors, neurinomas, and meningiomas).3,31 Fur- 6,28 right. Accordingly, we found a significantly larger jugular thermore, the nerves can be compromised iatrogenically dur- bulb on the right side in 60% of cases, whereas the inferior ing surgical treatment of such lesions.23,32 Thus, detailed petrosal sinus showed no significant difference in size from the knowledge of the JF, its contents, and adjacent cranial nerves is left to right sides. important for both radiologists and neurosurgeons. On the The inferior petrosal sinus interconnects the cavernous si- basis of our findings, we propose the combined use of CE- nus and the basilar venous plexus with the jugular bulb and FIESTA and CE-MRA as the ideal imaging protocol to depict courses on the intracranial surface of the petroclival fissure. the detailed in vivo anatomy of the JF, its content, and adjacent After entering the petrosal portion of the JF, the inferior petrosal sinus forms a plexiform confluence with the venous plexus structures that might facilitate the planning of surgical ap- of the hypoglossal canal, the inferior petroclival vein, and trib- proaches to that region. We included an illustrative case to utaries from the vertebral venous plexus and the posterior provide evidence for the potential of these sequences (Fig 8). condylar emissary vein. This confluence empties into the me- Further studies on patients with pathologies affecting the JF dial aspect of the jugular bulb through 1 or 2 openings most are necessary to prove the advantages of this protocol in clin- often between CNIX and CNX.1 CE-MRA enabled us to visu- ical settings.

AJNR Am J Neuroradiol ●:● ͉ ● 2009 ͉ www.ajnr.org 7 Conclusions 15. Yousry I, Moriggl B, Schmid UD, et al. Trigeminal ganglion and its divisions: detailed anatomic MR imaging with contrast-enhanced 3D constructive in- On the basis of our results, we propose the combined use of terference in the steady state sequences. AJNR Am J Neuroradiol CE-FIESTA and CE-MRA sequences as optimal imaging pro- 2005;26:1128–35 tocol for the analysis of the JF and its contents at 3T. This 16. Yagi A, Sato N, Taketomi A, et al. Normal cranial nerves in the cavernous sinuses: contrast-enhanced three-dimensional constructive interference in protocol is expected to aid in detecting and characterizing the steady state MR imaging. AJNR Am J Neuroradiol 2005;26:946–50 pathologic conditions of the JF and in planning the best safe 17. Yousry I, Camelio S, Wiesmann M, et al. Detailed magnetic resonance imaging surgical approach to lesions in the JF region. Further studies anatomy of the cisternal segment of the abducent nerve: Dorello’s canal and neurovascular relationships and landmarks. J Neurosurg 1999;91:276–83 on larger case series should be performed to confirm its value 18. Casselman JW, Kuhweide R, Deimling M, et al. Constructive interference in in pathologic conditions of the JF. steady state-3DFT MR imaging of the inner ear and cerebellopontine angle. AJNR Am J Neuroradiol 1993;14:47–57 19. Yousry I, Camelio S, Schmid UD, et al. Visualization of cranial nerves I-XII: References value of 3D CISS and T2-weighted FSE sequences. Eur Radiol 2000;10:1061–67 1. Rhoton AL. Jugular foramen. Neurosurgery 2000;47(suppl 3):267–85 20. Seitz J, Held P, Fru¨ndR,etal.Visualization of the IXth to XIIth cranial nerves 2. Tekdemir I, Tuccar E, Aslan A, et al. Comprehensive microsurgical anatomy of using 3-dimensional constructive interference in steady state, 3-dimensional the jugular foramen and review of terminology. J Clin Neurosci 2001;8:351–56 magnetization-prepared rapid gradient echo and T2-weighted 2-dimensional 3. Song MH, Lee HY, Jeon JS, et al. Jugular foramen schwannoma: analysis on its turbo spin echo magnetic resonance imaging sequences. J Neuroimaging origin and location. Otol Neurotol 2008;29:387–91 2001;11:160–64 4. Lachman N, Acland RD, Rosse C. Anatomical evidence for the absence of a 21. Wikstro¨m J, Ronne-Engstro¨m E, Gal G, et al. Three-dimensional time-of-flight morphologically distinct cranial root of the accessory nerve in man. Clin Anat (3D TOF) magnetic resonance angiography (MRA) and contrast-enhanced 2002;15:4–10 MRA of intracranial aneurysms treated with platinum coils. Acta Radiol 5. Rubinstein D, Burton BS, Walker AL. The anatomy of the inferior petrosal 2008;49:190–96 sinus, glossopharyngeal nerve, vagus nerve, and accessory nerve in the 22. Nael K, Fenchel M, Salamon N, et al. Three-dimensional cerebral contrast- jugular foramen. AJNR Am J Neuroradiol 1995;16:185–94 enhanced magnetic resonance venography at 3.0 Tesla: initial results using 6. Hatiboglu M, Anil A. Structural variations in the jugular foramen of the hu- highly accelerated parallel acquisition. Invest Radiol 2006;41:763–68 man skull. J Anat 1992;180:191–96 23. Ozveren MF, Tu¨re U, Ozek MM, et al. Anatomic landmarks of the glossopha- 7. Lang J. Jugular foramen. In: Lang J, ed. Clinical Anatomy of the Posterior Cranial ryngeal nerve: a microsurgical anatomic study. Neurosurgery 2003;52:1400–10 Fossa and Its Foramina. New York: Thieme Medical Publishers; 1991:92–96 24. Ryan S, Blyth P, Duggan N, et al. Is the cranial accessory nerve really a portion 8. Yousry I, Moriggl B, Schmid UD, et al. Detailed anatomy of the intracranial of the accessory nerve? Anatomy of the cranial nerves in the jugular foramen. segment of the hypoglossal nerve: neurovascular relationships and land- Anat Sci Int 2007;82:1–7 marks on magnetic resonance imaging sequences. J Neurosurg 2002;96: 25. Gopen Q, Rosowski JJ, Merchant SN. Anatomy of the normal human cochlear 1113–22 aqueduct with functional implications. Hear Res 1997;107:9–22 9. Davagnanam I, Chavda SV. Identification of the normal jugular foramen and 26. Rask-Andersen H, Stahle J, Wilbrand H. Human cochlear aqueduct and its lower cranial nerve anatomy: contrast-enhanced 3D fast imaging employing accessory canals. Ann Otol Rhinol Laryngol Suppl 1977;86:1–16 steady-state acquisition MR imaging. AJNR Am J Neuroradiol 2008;29:574–76. 27. Guild SR. Glomus jugulare, a nonchromaffin paraganglion in man. Ann Otol Epub 2007 Dec 7 Rhinol Laryngol 1953;62:1045–71 10. Daniels DL, Williams AL, Haughton VM. Jugular foramen: anatomic and com- 28. Dichiro G, Fisher RL, Nelson KB. The jugular foramen. J Neurosurg puted tomographic study. AJR Am J Roentgenol 1984;142:153–58 1964;21:447–60 11. Lo WW, Solti-Bohman LG. High-resolution CT of the jugular foramen: anat- 29. Lang J. Veins and dural sinuses. In: Von Lanz T, Wachsmuth W, eds. Practical omy and vascular variants and anomalies. Radiology 1984;150:743–47 Anatomy: Part I—Head. Berlin, Germany: Springer-Verlag; 2004:578–633 12. Chong VF, Fan YF. Radiology of the jugular foramen. Clin Radiol 30. Bhuller A, Sanudo JR, Choi D, et al. Intracranial course and relations of the 1998;53:405–16 hypoglossal nerve: an anatomic study. Surg Radiol Anat 1998;20:109–12 13. Daniels DL, Schenck JF, Foster T, et al. Magnetic resonance imaging of the 31. Ramina R, Maniglia JJ, Fernandes YB, et al. Tumors of the jugular foramen: jugular foramen. AJNR Am J Neuroradiol 1985;6:699–703 diagnosis and management. Neurosurgery 2005;57(suppl 1):59–68 14. Daniels DL, Czervianke LF, Pech P. Gradient recalled echo MR imaging of the 32. Roche PH. Mercier P, Sameshima T, et al. Surgical anatomy of the jugular jugular foramen. AJNR Am J Neuroradiol 1988;9:675–78 foramen. Adv Tech Stand Neurosurg 2008;33:233–63

8 Linn ͉ AJNR ● ͉ ● 2009 ͉ www.ajnr.org